Skip to main content

Reproductive Organ Development in the Ivory Shell Babylonia japonica and the Rock Shell Thais clavigera

  • Chapter
  • First Online:
Biological Effects by Organotins

Abstract

Results of histological examination of normal differentiation and development of the genital tract and gonad in the ivory shell Babylonia japonica (Buccinidae) are described. The formation of male-type genitalia (penis and vas deferens) in imposex-exhibiting females seems to mimic the normal development of male genitalia in prosobranch gastropods, on the basis of observations using a wild-caught 2-year-old specimen and laboratory-reared juveniles aged 0–24 months. Gonad differentiation was unclear before age 14 months but progressed after 16 months. Both sexes had a complete genital tract and mature gonads at 20 months. However, differentiation and development occurred earlier in females than in males. Development of the genital tract preceded gonad differentiation. Vas deferens morphogenesis in males resembled that in imposex-exhibiting females. Histological examination of the development of male genitalia in imposex-exhibiting female rock shells, Thais clavigera (Muricidae), using specimens from a wild population and tributyltin (TBT)-exposed females in the laboratory, allowed observation of a variety of vas deferens morphogenesis patterns. Taking into consideration observed results both from wild female specimens and from TBT-exposed females in the laboratory, the vas deferens sequence (VDS) index for T. clavigera has been proposed as VDS 1–6, which is a little different from that for Nucella lapillus. Comparison of the differentiation and development of male genitalia in normal males and imposex-exhibiting females among gastropod species implies it does not seem to be strictly regulated: relatively large variation in the differentiation and development of genitalia could occur among individuals, as well as among species of prosobranch gastropods.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AFS Convention:

the International Convention on the Control of Harmful Anti-fouling Systems on Ships

DMSO:

dimethyl sulfoxide

EDCs:

endocrine-disrupting chemicals

H&E:

hematoxylin and eosin

IMO:

International Maritime Organization

OECD:

Organization for Economic Co-operation and Development

9cRA:

9-cis retinoic acid

RXR:

retinoid X receptor

TBT:

tributyltin

TBTCl:

tributyltin chloride

TPhT:

triphenyltin

VDS index:

vas deferens sequence index

References

  • Bryan GW, Gibbs PE, Hummerstone LG et al (1986) The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. J Mar Biol Assoc UK 66:611–640

    Article  CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR et al (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. J Mar Biol Assoc UK 67:525–544

    Article  CAS  Google Scholar 

  • Bryan GW, Gibbs PE, Burt GR (1988) A comparison of the effectiveness of tri-n-butyltin chloride and five other organotin compounds in promoting the development of imposex in the dog-whelk, Nucella lapillus. J Mar Biol Assoc UK 68:733–744

    Article  CAS  Google Scholar 

  • Castro LFC, Lima D, Machado A et al (2007) Imposex induction is mediated through the retinoid X receptor signalling pathway in the neogastropod Nucella lapillus. Aquat Toxicol 85:57–66

    Article  CAS  Google Scholar 

  • Gibbs PE, Bryan GW (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 66:767–777

    Article  CAS  Google Scholar 

  • Gibbs PE, Bryan GW (1996) TBT-induced imposex in neogastropod snails: masculinization to mass extinction. In: de Mora SJ (ed) Tributyltin: case study of an environmental contaminant. Cambridge University Press, Cambridge, pp 212–236

    Chapter  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al (1987) The use of the dog-whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. J Mar Biol Assoc UK 67:507–523

    Article  CAS  Google Scholar 

  • Gibbs PE, Pascoe PL, Burt GR (1988) Sex change in the female dog-whelk, Nucella lapillus, induced by tributyltin from antifouling paints. J Mar Biol Assoc UK 68:715–731

    Article  Google Scholar 

  • Gibbs PE, Bryan GW, Pascoe PL et al (1990) Reproductive abnormalities in female Ocenebra erinacea (Gastropoda) resulting from tributyltin-induced imposex. J Mar Biol Assoc UK 70:639–656

    Article  Google Scholar 

  • Gilbert SF (2006) Sex determination; chromosomal sex determination. In: Wigg C (ed) Developmental biology, 8th edn. Sinauer, Sunderland, pp 530–542

    Google Scholar 

  • Hamada F, Kanazawa T, Yamamoto E (1988) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefect Fish Exp Sta 6:110–116

    Google Scholar 

  • Hamada F, Kanazawa T, Yamamoto E (1989) Seed production of the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefect Fish Exp Sta 7:103–109

    Google Scholar 

  • Heyman RA, Mangelsdorf DJ, Dyck JA et al (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68:397–406

    Article  CAS  Google Scholar 

  • Horiguchi T (1993) Imposex caused by organotin compounds in marine gastropods from Japan (PhD Thesis, in Japanese). The University of Tokyo, Bunkyo-ku

    Google Scholar 

  • Horiguchi T (2009) Mechanism of imposex induced by organotins in gastropods. In: Arai T, Harino H, Ohji M, Langston WJ (eds) Ecotoxicology of antifouling biocides. Springer, Tokyo, pp 111–124

    Chapter  Google Scholar 

  • Horiguchi T, Shimizu M (1992) Effects on aquatic organisms, mainly on molluscs. In: Satomi Y, Shimizu M (eds) Organotin pollution and its effects on aquatic organisms. Koseisha-Koseikaku, Tokyo, pp 99–135 [in Japanese]

    Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1994) Imposex and organotin compounds in Thais clavigera and T. bonni in Japan. J Mar Biol Assoc UK 74:651–669

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1995) Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from antifouling paints. Mar Pollut Bull 31:402–405

    Article  CAS  Google Scholar 

  • Horiguchi T, Shiraishi H, Shimizu M et al (1997) Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera. Environ Pollut 95:85–91

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Kaya M et al (2002) Tributyltin and triphenyltin induce spermatogenesis in ovary of female abalone, Haliotis gigantea. Mar Environ Res 54:679–684

    Article  CAS  Google Scholar 

  • Horiguchi T, Kojima M, Hamada F et al (2006) Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect 114(suppl 1):13–19

    Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2007) Retinoid X receptor gene expression and protein content in tissues of the rock shell Thais clavigera. Aquat Toxicol 84:379–388

    Article  CAS  Google Scholar 

  • Horiguchi T, Ohta Y, Nishikawa T et al (2008) Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol Toxicol 24:553–562

    Article  Google Scholar 

  • Horiguchi T, Nishikawa T, Ohta Y et al (2010a) Time course of expression of the retinoid X receptor gene and induction of imposex in the rock shell, Thais clavigera, exposed to triphenyltin chloride. Anal Bioanal Chem 396:597–607

    Article  CAS  Google Scholar 

  • Horiguchi T, Urushitani H, Ohta Y et al (2010b) Establishment of a polyclonal antibody against the retinoid X receptor of the rock shell Thais clavigera and its application to rock shell tissues for imposex research. Ecotoxicology 19:571–576

    Article  CAS  Google Scholar 

  • Horiguchi T, Ohta Y, Urushitani H et al (2012a) Vas deferens and penis development in the imposex-exhibiting female rock shell, Thais clavigera. Mar Environ Res 76:71–79

    Article  CAS  Google Scholar 

  • Horiguchi T, Lee JH, Park JC et al (2012b) Specific accumulation of organotin compounds in tissues of the rock shell, Thais clavigera. Mar Environ Res 76:56–62

    Article  CAS  Google Scholar 

  • Horiguchi T, Ohta Y, Hamada F et al (2014) Development of reproductive organs in the ivory shell Babylonia japonica: observations from wild populations and laboratory-reared juveniles. Mar Environ Res 93:4–14

    Article  CAS  Google Scholar 

  • International Maritime Organization (IMO) (2001) International convention on the control of harmful antifouling systems on ships (AFS/CONF/26). International Maritime Organization, London

    Google Scholar 

  • Jost A, Vigier B, Prépin J et al (1973) Studies on sex differentiation in mammals. Recent Prog Horm Res 29:1–41

    CAS  Google Scholar 

  • Kajikawa A, Yamamoto E, Masutani R (1983) Sexual characteristics and spawning abilities in the ivory shell, Babylonia japonica Reeve (in Japanese). Bull Tottori Prefect Fish Exp Station 1:16–18

    Google Scholar 

  • Levin AA, Sturzenbecker LJ, Kazmer S et al (1992) 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXR alpha. Nature (Lond) 355:359–361

    Article  CAS  Google Scholar 

  • Mangelsdorf DJ, Evans RM (1995) The RXR heterodimers and orphan receptors. Cell 83:841–850

    Article  CAS  Google Scholar 

  • Mangelsdorf DJ, Borgmeyer U, Heyman RA et al (1992) Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes Dev 6:329–344

    Article  CAS  Google Scholar 

  • Morris-Kay GM (1997) Retinoids in mammalian embryonic development. In: Sherbet GV (ed) Retinoids: their physiological function and therapeutic potential. JAI Press, Greenwich, pp 79–93

    Chapter  Google Scholar 

  • Nishikawa J, Mamiya S, Kanayama T et al (2004) Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods. Environ Sci Technol 38:6271–6276

    Article  CAS  Google Scholar 

  • [OECD] Organisation for Economic Co-operation and Development (2016) http://www.oecd-ilibrary.org/environment/oecd-guidelines-for-the-testing-of-chemicals-section-2-effects-on-biotic-systems_20745761

  • Redfern CPF (1997) Molecular mechanisms of the retinoid function. In: Sherbet GV (ed) Retinoids: their physiological function and therapeutic potential. JAI Press, Greenwich, pp 35–77

    Chapter  Google Scholar 

  • Scott AP (2012) Do mollusks use vertebrate sex steroids as reproductive hormones? Part I: Critical appraisal of the evidence for the presence, biosynthesis and uptake of steroids. Steroids 77:1450–1468

    Article  CAS  Google Scholar 

  • Scott AP (2013) Do mollusks use vertebrate sex steroids as reproductive hormones? II. Critical review of the evidence that steroids have biological effects. Steroids 78:268–281

    Article  CAS  Google Scholar 

  • Smith BS (1971) Sexuality in the American mud snail, Nassarius obsoletus Say. Proc Malacol Soc Lond 39:377–378

    Google Scholar 

  • Sternberg RM, Hotchkiss AK, Leblanc GA (2008) Synchronized expression of retinoid X receptor mRNA with reproductive tract recrudescence in an imposex-susceptible mollusc. Environ Sci Technol 42:1345–1351

    Article  CAS  Google Scholar 

  • Stroben E, Schulte-Oehlmann U, Fioroni P et al (1995) A comparative method for easy assessment of coastal TBT pollution by the degree of imposex in prosobranch species. Haliotis 24:1–12

    Google Scholar 

  • Urushitani H, Katsu Y, Ohta Y et al (2011) Cloning and characterization of retinoid X receptor (RXR) isoforms in the rock shell, Thais clavigera. Aquat Toxicol 103:101–111

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshihiro Horiguchi Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Japan

About this chapter

Cite this chapter

Horiguchi, T. (2017). Reproductive Organ Development in the Ivory Shell Babylonia japonica and the Rock Shell Thais clavigera . In: Horiguchi, T. (eds) Biological Effects by Organotins. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56451-5_11

Download citation

Publish with us

Policies and ethics